1 1 2 Comparative behavior of red lionfish (Pterois volitans) on native
Pacific vs. invaded Atlantic coral reefs
3 4 5 6 7 8 9 10 11 12 13 14 Running head: Native vs. invasive lionfish behavior
Katherine Cure1,2,*, Cassandra E. Benkwitt3, Tye L. Kindinger3, Emily A. Pickering3,
Timothy J. Pusack3, Jennifer L. McIlwain1,4, Mark A. Hixon3
1 The Marine Laboratory, University of Guam, Mangilao, Guam 96923, USA
2 Present address: School of Plant Biology, The University of Western Australia, Crawley, WA
6009, Australia
3 Department of Zoology, Oregon State University, Corvallis, OR 97331-2914, USA
4 Department of Environment and Agriculture, Curtin University, Perth, WA 6845, Australia
15 16 *katherine.cure@gmail.com
17 ABSTRACT: Pacific red lionfish (Pterois volitans) have invaded Atlantic reefs and reached
18 much greater population densities than on native reefs. We hypothesized that lionfish on invaded
19 reefs would (1) experience higher kill rates and thus spend less time hunting, given the naïveté of
20 Atlantic prey, (2) consume a greater variety of prey, given the lack of native prey defenses, and
21 (3) display less pronounced crepuscular patterns of hunting, given the ease of capturing Atlantic
22 prey. Comparative behavioral observations were conducted in two native regions (Philippines
23 and Guam) and two invaded regions (Cayman Islands and Bahamas) to assess lionfish time
24 budgets and diurnal activity patterns, and to explore correlations between environmental
25 variables and lionfish behavior. Contrary to our first hypothesis, total time allocated to hunting
26 and kill rates showed no difference between native and invaded reefs, despite considerable
27 regional variation. However, Atlantic prey of lionfish were twice as large as Pacific prey,
28 suggesting that despite similar hunting behavior, invasive lionfish are receiving greater
29 nutritional input. Furthermore, consistent with our second hypothesis, lionfish on invaded reefs
2 30 had broader diets, and also relied less on "blowing" behavior for prey capture, pointing to
31 substantial prey naïveté in the invaded range. Importantly, only in the invaded range did we
32 observe lionfish consuming parrotfishes, the decline of which could have indirect effects on
33 interactions between seaweeds and corals. Finally, lionfish overall tended to exhibit a
34 crepuscular pattern in behavior whereby hunting peaked at sunrise and/or sunset, with no
35 differences attributable to native vs. invasive status.
36 37 KEY WORDS: Native vs. invasive behavior; Diurnal hunting pattern; Crepuscular hunting;
38 Time budget
39 40 INTRODUCTION
41 In the mid 1980´s Pacific red lionfish (Pterois volitans) invaded the Western Atlantic via the
42 aquarium trade (Semmens et al. 2004), and beginning in the early 2000´s extended their range
43 throughout the Caribbean, Gulf of Mexico, and down the South American coastline (Schofield
44 2010). Despite local attempts at removal, invasive lionfish reached local population densities far
45 greater than in their native Pacific (Whitfield et al. 2007, Green & Côté 2008, Kulbicki et al.
46 2012). At invaded locations, lionfish consume a broad diversity of small fishes and crustaceans
47 including juveniles of herbivores (Morris & Akins 2009) and have caused substantial reductions
48 in the recruitment and abundance of reef fishes (Albins & Hixon 2008, Green et al. 2012).
49 Invasive lionfish can also negatively affect native piscivorous predators through both predation
50 on juveniles and competition with adults (Albins 2012). Thus, lionfish may ultimately cause
51 drastic changes in Atlantic coral-reef ecosystems (Albins & Hixon 2011).
3 52 Lionfish are likely protected from predators by their cryptic coloration and numerous
53 venomous spines (Allen & Eschemeyer 1973). Predators rarely target adult lionfish at either
54 native or invaded locations, despite anecdotal evidence of occasional predation (Bernadsky &
55 Goulet 1991, Maljkovic & Van Leeuwen 2008). Because natural controls have not been
56 definitively identified at either the native Pacific or invaded Atlantic, direct removals of lionfish
57 by humans have to date been the only effective way to reduce invasive populations. Because
58 invasive lionfish are widespread geographically and occur far deeper than usual SCUBA depths
59 (Whitfield et al. 2007, Lesser & Slattery 2011), complete eradication is unlikely.
60 Before the invasion, little was known about the ecology and behavior of lionfish, due in part
61 to their rarity in their native range (Kulbicki et al. 2012). Lionfish use two types of hunting
62 methods: slow stalking of prey aided by fanlike pectoral fins that herd prey, and sit-and-wait
63 ambush (Randall 2005). Blowing behavior, by which lionfish produce jets of water directed at
64 prey while approaching them, enhances predatory efficiency by confusing or distracting prey
65 (Albins & Lyons 2012). Lionfish diets are well documented in the invasive range and include a
66 broad variety of coral reef fishes, crustaceans (Morris & Akins 2009, Côté & Maljkovic 2010,
67 Green et al. 2012), and even conspecifics (Valdez-Moreno et al. 2012). These records coincide
68 with diet reported from qualitative descriptions in the native range (Myers 1999). Hunting takes
69 place during crepuscular periods (Myers 1999, Randall 2005) when low light levels impede
70 visually adapted prey (Helfman 1986). During the daytime, native lionfish become inactive in
71 holes and crevices (Fishelson 1997), a pattern common to a variety of other predatory fishes and
72 often influenced by ambient light levels (Belovsky & Slade 1986). Invasive lionfish in the
73 Bahamas also display this crepuscular pattern of hunting behavior (Green et al. 2011).
4 74 Behavioral comparisons between populations in native vs. invaded ranges are highly
75 informative because they may identify factors that foster invasion success (Holway & Suarez
76 1999, Morris & Whitfield 2009, Meyer & Dierking 2011), and may help in developing control
77 measures (Guo 2006). Changes in diel activity of fishes are a common response to differences in
78 biotic and abiotic environmental factors, including predator abundance, prey availability,
79 presence/absence of competitors, habitat structure, depth, and abiotic conditions such as
80 temperature and light levels (Chen et al. 1999, Reebs 2002, Hansen et al. 2004, Andrews et al.
81 2009, Côté & Maljkovic 2010).
82 invasion is often accompanied by release from the natural controls of competition and predation
83 (Mack et al. 2000), behavioral differences in invasive species are therefore likely between native
84 and invaded locations. For invasive predators, such differences can mean access to more
85 abundant or higher quality prey (Meyer & Dierking 2011), enhanced by the substantial
86 advantages novel invasive predators usually have over native naïve prey (Cox & Lima 2006).
Because these factors may vary regionally, and because
87 We conducted replicate comparative field observations in two regions in the native Pacific
88 Ocean and two regions in the invaded Atlantic Ocean in an effort to determine whether there are
89 any inter-ocean differences in lionfish behavior. Assuming native Atlantic prey are naïve to
90 invasive lionfish, we hypothesized that lionfish would have higher success at killing prey at
91 invaded regions. If so, we further hypothesized that higher success at killing prey would result in
92 concomitant changes to predatory behavior in the invaded Atlantic, including less time spent
93 hunting as lionfish satiated more rapidly, and hunting being less restricted to the low-light levels
94 of crepuscular times often exploited by native predators (Helfman 1986). We also predicted that,
95 as an efficient and voracious generalist predator, lionfish would consume a greater variety of
96 prey in their invaded Atlantic range compared to their native Pacific range.
5 97 98 MATERIALS AND METHODS
99 Data collection
100 We observed in situ behavior of lionfish in two regions within each ocean: the Philippines
101 and Guam in the native range, and the Cayman Islands and the Bahamas in the invaded range
102 (Fig. 1). Invasive lionfish were first detected in the Bahamas in 2004 and in the Caymans in 2008
103 (Schofield 2009). Sampling was conducted over a 3-year period, mostly during June to
104 September 2009-2011. We selected sites known to have lionfish, including sandy slopes with
105 coral patches, continuous reef walls, and a few artificial habitats (e.g., piers, small wrecks, tire
106 reefs, and old fish traps). Maximum depth at these sites was 25 m.
107 The number of sites sampled depended on lionfish frequency encountered at those sites. In
108 the native range, where the probability of encountering lionfish was low, 20 sites were sampled
109 in the Philippines and 13 on Guam. In the invasive range, 5 sites were sampled in the Bahamas
110 and 4 in the Cayman Islands.
111 Because capturing and tagging lionfish observed in this study was logistically impractical,
112 and because tagging can possibly alter lionfish behavior towards the observer (personal
113 observation), we chose to observe untagged animals. At each site during any given time of day,
114 we ensured that different animals were sampled by swimming over the site unidirectionally and
115 sampling lionfish encountered haphazardly along the way. Each site was sampled only once
116 within a day, and if we returned to that same site on another day, we sampled different parts of
117 the site and different time periods. Therefore, we assumed that our observations were statistically
118 independent and representative, even when we had no way of knowing with certainty whether
119 we resampled the same fish between days.
6 120 In each region, we conducted a series of standardized ten-minute observations taken from
121 sunrise to sunset (between ~0600 and ~1830 h). During each period, lionfish behavior was
122 recorded by trained observers using either SCUBA or snorkel. There were 5 observers in the
123 native range and 8 in the invaded range (1 observer in the Pacific and 2 observers in the Atlantic
124 completed 60% of the total observations). Care was taken to minimize the influence of observer
125 presence on lionfish behavior by keeping a distance of approximately 3 m from each fish. We
126 attempted to sample equally all times of day, sites, habitats and environmental conditions,
127 subject to logistic constraints.
128 Eight lionfish behaviors were quantified, following an initial ethogram constructed from a
129 pilot study in the Bahamas. Behaviors were quantified as either proportion of time (i.e.
130 proportion of each 10 minute observation period) or counts (i.e. number of events per each 10
131 minute observation period). Proportion of time was recorded for each of four activities: inactive,
132 minimal activity, active, and hunting. The first three range from lionfish being stationary, to
133 short distance movements, to long distance movements, respectively, but in all instances pectoral
134 fins are relaxed (i.e. not flared and in position for hunting). Hunting activity was obvious as
135 lionfish focused on particular prey with fully flared pectoral fins (Green et al. 2011). Counts
136 were recorded for aggressive interactions (chasing other lionfish or other fish species), strikes
137 (successful and unsuccessful attacks on potential prey), kills (successful capture of prey, i.e. prey
138 consumed), and blows (water current directed at prey). During each observation period, we
139 identified all prey approached by lionfish to at least the family level as well as the species level
140 where possible, and estimated prey body size as total length (TL) to the nearest cm.
141 For each 10-min observation we also measured five environmental variables known to
142 influence fish behavior. (i) We recorded the microhabitat within which each observation
7 143 occurred, mostly hard coral, rock-boulder/cave and sand/rubble, and less frequently seagrass
144 beds, sponge fields, soft coral fields, and artificial structures. Lionfish usually did not move
145 outside of the identified microhabitat during the observation time. In the few cases where such
146 movement did occur, microhabitat was classified as the area where lionfish spent most of the
147 observation time. During each sample period, we also recorded (ii) cloud cover (clear: 0 to 25%,
148 partly cloudy: 25 to 75%, overcast: >75%), (iii) current (low: diver barely kicking to maintain
149 position, medium: periodic kicking required by diver to maintain position, high: constant kicking
150 by diver required to maintain position), (iv) estimated lionfish size (TL) and (v) depth.
151 Temperature was measured in situ using HOBO® temperature loggers every 30 min in Guam
152 and the Bahamas, while temperature data for the Philippines and the Cayman Islands were
153 recorded
154 (http://coralreefwatch.noaa.gov/satellite/current/products_vs.html). 155 Statistical analyses
from
NOAA
virtual
stations
156 Frequency distributions for each of the quantified behaviors were highly skewed and had
157 high proportions of ones and zeros, so data transformation did not result in either normality or
158 homoscedasticity. The two most common behaviors (inactive and hunting), were therefore
159 analyzed with a logistic regression using a generalized linear mixed-effects model (GLMM), in
160 which region (random effect) was nested within ocean (fixed effect). The model was robust to
161 the skewed nature of the data and allowed us to explore the cumulative effects of putative
162 explanatory variables. Cumulative effects of ocean, time period, habitat, cloud cover, current,
163 lionfish size (TL), and depth on lionfish behavior, were assessed.
164 Despite the reduction in detail from the conversion of proportions to binary data, a logistic
165 regression model was chosen in part because a lionfish that is exhibiting inactivity or hunting is
8 166 doing so exclusively (i.e., if a lionfish is inactive, it cannot hunt, and vice versa). The behaviors
167 categorized as “minimal activity” and “active” (both not involving hunting) accounted for less
168 than 10% of the total time budgets for all regions, so these were excluded from further analysis,
169 as well as rates of aggressive behavior toward conspecifics, which were very low in all regions.
170 Data for y were binary variables created for lionfish behavior (0 = inactive and 1 = hunting).
171 An observation was considered as inactive if >50% of the ten minute period was spent inactive,
172 and as hunting if >50% of the ten minutes were spent hunting; 75% of all observation periods
173 were dominated by one behavior or the other (i.e. either hunting or inactive represented >80% of
174 the observation period). All logistic regressions were done in R (R Development Core Team
175 2010) using the package “lme4” (Bates et al. 2011) and following the guidelines of Rossiter &
176 Loza (2010) and Peng et al. (2002). Model fit was assessed by examination of model residuals,
177 predicted outcomes, likelihood ratio tests and chi-square statistics (Quinn & Keough 2002).
178 Validation of the model by comparing predicted probabilities to observed outcomes was also
179 performed (70% of outcomes were correctly predicted by the model).
180 Partitioning of variance to determine the relative importance of each explanatory variable in
181 the model was calculated using the R package “hier.part” (Walsh & MacNally 2008).
182 Hierarchical partitioning is a technique that, rather than seeking a best fit, uses all possible
183 models in a regression hierarchy to distinguish variables that have the highest independent
184 correlations with the response variable; these variables are most likely to influence variation
185 (MacNally 1996).
186 One-way univariate permutational analyses of variance (PERMANOVA, Anderson et al.
187 2008) were used to compare strike and kill rate means at the level of ocean vs. ocean, with region
188 nested within ocean. These were chosen because of their robustness to deviations from normality
9 189 and homoscedasticity, characteristic of our data. PERMANOVAs were run for 9999
190 permutations in PRIMER 6 (PRIMER-E Ltd., 2009) with the following specifications:
191 Euclidean distance, sequential sums of squares, and permutation of residuals under the reduced
192 model (Anderson et al. 2008).
193 194 RESULTS
195 We observed lionfish ranging in size from 5 to 35 cm TL during a total of 192 hours of time
196 budgeting at native reefs (Philippines 37 hr, Guam 28 hr) and invaded reefs (Cayman Islands 73
197 hr, Bahamas 54 hr). Variation in lionfish time budgets was not substantial between oceans, but
198 considerable between regions within each ocean (Fig. 2, Table 1). Lionfish were usually more
199 active in the Philippines (native) and the Cayman Islands (invaded), and more sedentary in Guam
200 (native) and the Bahamas (invaded). In all regions, we never observed predators attacking
201 lionfish. Temperature was similar both between oceans (pooling regional means ±SE: Pacific =
202 28.13 ± 0.02 °C, Atlantic = 28.69 ± 0.01 °C) and between regions within oceans (mean ± SE:
203 Philippines = 30.23 ± 0.04 °C, Guam = 28.12 ± 0.01 °C, Cayman Islands = 29.72 ± 0.06 °C,
204 Bahamas = 28.68 ± 0.02 °C).
205 Hunting behavior and prey consumed
206 Lionfish hunting behavior contradicted a priori expectations of inter-ocean differences. Time
207 spent hunting throughout the day was equal between the Atlantic and the Pacific (Table 1),
208 although maximum hunting time was nonetheless observed in the Pacific (Philippines = 70%
209 hunting) and minimum hunting time in the Atlantic (Bahamas = 17.6% hunting) (Fig. 2). Diurnal
210 patterns of lionfish behavior showed that, irrespective of native vs. invaded range, hunting was
211 greater and inactivity lower during sunrise and/or sunset (Fig. 3, Table 1). A strongly crepuscular
10 212 hunting pattern was most evident for lionfish in Guam and the Bahamas, while lionfish hunting
213 in the Philippines and the Cayman Islands peaked at sunrise (Fig. 3, A & C).
214 Also contradicting expectations, both strike and kill rates were similar between oceans
215 (Strikes: Pseudo-F = 0.051, df = 1,1146, p = 1; Kills: Pseudo-F = 0.081, df = 1,1146, p = 0.834)
216 (Fig. 4A), although there was considerable regional variation. Successful kill rates (% of total
217 strikes that resulted in prey being consumed = [number of kills / number of strikes]*100) were
218 highest in the Bahamas (51.2%), followed by Philippines (50.0%), the Cayman Islands (25.6%),
219 and Guam (22.9%) (Fig. 4A).
220 Despite lionfish time budgets and kill rates varying more between regions than between
221 oceans, there were several clear differences in hunting behavior between the native Pacific and
222 invaded Atlantic ranges. First, mean blowing rates were three times lower in the invaded range
223 vs. the native range (Fig. 4B). Second, mean prey size was nearly double in the invaded vs. the
224 native range (mean  SEM: Atlantic = 2.45  0.42 cm, Pacific = 1.50  0.35 cm). Third,
225 observed diets (kill rates) were broader in the invaded range than in the native range (total # of
226 prey taxa killed/1000 min: Atlantic = 1.6, Pacific = 0.9), even though strikes targeted a greater
227 diversity of fishes in the native Pacific (total # of prey taxa targeted/1000 min: Atlantic = 2.5,
228 Pacific = 3.8). Lionfish successfully killed prey in 6 fish families in the invaded range
229 (Apogonidae, Blenniidae, Gobiidae, Labridae, Pomacentridae and Scaridae), vs. only 2 in the
230 native range (Pomacentridae and Trichonotidae) (Table 2). Strikes were mostly towards gobies
231 (Gobiidae), wrasses (Labridae) and parrotfishes (Scaridae) in the invaded range, and towards
232 cardinalfishes (Apogonidae), gobies, and marine catfishes (Plotosidae) in the native Pacific.
233 Successful kills in the Atlantic included ecologically important species such as juvenile
234 parrotfishes, which were not targeted by lionfish in the Pacific. These differences in diet breadth
11 235 occurred despite the fact that there are far more potential prey fish species in the native range
236 compared to the invaded range of lionfish (Roberts et al. 2002).
237 Lionfish size
238 Overall, body size had no statistical effect on lionfish behavior (Table 1). However, the
239 coefficient estimate for size was negative, suggesting that smaller lionfish spent more time
240 hunting (β = -0.014, p = 0.102, Table 1). Furthermore, when individual regions were analyzed
241 separately, smaller lionfish (5 to 15 cm TL) in the Philippines and the Cayman Islands spent
242 more time hunting than larger fish (Spearman Rank Correlations: ῤ = -0.145, p = 0.040 for the
243 Philippines; ῤ = -0.131, p = 0.036 for the Cayman Islands). Lionfish size distributions differed
244 across regions, with larger lionfish found in Guam and the Bahamas (mean ± SD: Philippines =
245 17.69 ± 6.15 cm TL, Guam = 22.08 ± 7.22 cm TL, Cayman Islands = 15.63 ± 5.57 cm TL,
246 Bahamas = 22.66 ± 5.44 cm TL; Kruskal-Wallis H = 219.191, df = 3, 1146, p < 0.001).
247 Environmental effects
248 Between-ocean comparisons revealed that native Pacific and invasive Atlantic lionfish
249 responded similarly to measured environmental factors (Table 1). Hunting activity was greatest
250 when overcast (Table 1), and this response to changes in cloud cover was most evident for
251 lionfish on Guam and the Bahamas (Fig. 5A). Together with the Caymans, these two regions
252 were sampled at shallower depths (mean ± SEM: Philippines = 19.3 ± 0.3 m, Guam = 10.9 ± 0.4
253 m, Cayman Islands = 9.4 ± 0.3 m, Bahamas = 3.1 ± 0.1 m; Kruskal-Wallis H = 925.1, df = 3,
254 1146, p < 0.001), where the effects of cloud cover on ambient light levels were most obvious to
255 the observers. High currents had a consistent effect across all regions, resulting in less time spent
256 hunting and greater inactivity when compared to both low and medium currents (Table 1),
257 especially on Guam (Fig. 5B). Habitat had only slightly significant effects in both inactivity and
12 258 hunting patterns (Table 1, Fig. 5C). However, lionfish in rock-boulder habitats tended to hunt
259 less and be more inactive, in contrast to lionfish over hard coral and sand/ rubble, where hunting
260 peaked, especially in the Atlantic (Fig. 5C).
261 When all variables were examined simultaneously, hierarchical partitioning analyses
262 indicated that time-of-day, followed by depth and habitat, were most important in explaining
263 variation in lionfish behavior (Fig. 6). Although coefficient estimates for depth in the logistic
264 model were not significant, depth accounted for almost 20% of total model deviance (Fig. 6) and
265 coefficient estimates indicated a trend towards greater time spent hunting with increasing depth
266 (ß = 0.028, p = 0.499) (Table 1).
267 268 DISCUSSION
269 Despite initial expectations of interoceanic differences in lionfish behavior related to
270 native vs. invasive status, our field observations from two regions in each of two oceans suggest
271 that overall patterns in lionfish time budgets, daily activity patterns, and success rates at killing
272 prey are similar in the native Pacific and the invaded Atlantic. These results show that if ease of
273 prey capture is higher for invasive lionfish due to naïve prey, this is not reflected in either kill
274 rates, hunting time or crepuscular hunting patterns.
275 Instead, lionfish behavioral patterns are determined more by regional differences in a
276 suite of environmental factors, which act synergistically to affect behavior. The most pronounced
277 of these factors was the low light level associated with crepuscular times, during which time
278 spent hunting was maximal, regardless of ocean of residence. Twilight foraging is a feature
279 common among coral-reef piscivores, and is probably related to the advantages that low light
280 levels confer to predators vs. their prey (Helfman 1986). The largely crepuscular hunting pattern
13 281 found, despite peaks occurring in either sunrise and sunset (Guam and Bahamas) or sunrise alone
282 (Philippines and Caymans), confirms earlier descriptions of lionfish in both their native range
283 (Fishelson 1975, Myers 1999) and invaded range (Green et al. 2011).
284 Between-ocean differences
285 While lionfish time budgets and kill rates did not vary appreciably between oceans, there
286 were nonetheless differences in diet breadth, prey size and use of blowing behavior between the
287 native and invaded ranges. Although coral-reef fishes are far more diverse in the Pacific than in
288 the Atlantic (Roberts et al. 2002), we observed invasive lionfish successfully consuming a
289 broader diversity of fishes in the Atlantic than native lionfish in the Pacific. Diet was broader in
290 the Atlantic despite the fact that lionfish strikes were directed at a greater diversity of prey in the
291 Pacific. Atlantic prey species composition was similar to that previously observed in Bahamian
292 lionfish (Albins & Hixon 2008, Morris & Akins 2009). We observed only invasive lionfish
293 consuming parrotfishes (Scaridae). Parrotfishes are ecologically important herbivores that help to
294 keep seaweeds from overgrowing corals (Mumby 2006). Declines in such herbivores in the
295 invaded range could have severe indirect effects on Atlantic coral reefs (Albins and Hixon 2011).
296 There are at least three possible (not mutually exclusive) explanations for increased diet
297 breadth in invasive relative to native lionfish. The first is based on optimal foraging theory,
298 which predicts that diet breadth is determined by the encounter rate of preferred prey (Stephens
299 & Krebs 1986). It is possible that crustaceans and juvenile pomacentrids are preferred prey in the
300 Pacific and are present in sufficiently high densities that diet breadth is reduced in native Pacific
301 lionfish. The higher availability of fish recruits during the dates we sampled in the Philippines
302 (Abesamis & Russ 2010) compared to other regions is consistent with this hypothesis, yet the
14 303 fact that lionfish targeted a greater diversity of prey in the Pacific but successfully killed a lower
304 diversity of prey, tends to falsify this hypothesis.
305 A second explanation is that prey are naïve to lionfish as a novel predator in the newly
306 invaded Atlantic, allowing generalist lionfish to successfully capture a broader diversity of prey,
307 even when kill rates and hunting times were equal between native and invaded locations. This
308 explanation goes in line with our initial hypothesis that invasive lionfish would consume greater
309 variety of prey given the lack of native prey defenses. As observed for invasive lionfish (Albins
310 & Hixon 2008, Green et al. 2011), native prey may exhibit weak or nonexistent responses to
311 newly introduced predators (Cox & Lima 2006, Smith et al. 2008). Lionfish are new to the
312 Atlantic and do not resemble any native Atlantic predators. Therefore, prey types that normally
313 may not be available to native Pacific lionfish are present in invasive lionfish diet. Our findings
314 of broader targeted species in the native Pacific Ocean, yet greater success at killing more
315 diverse prey in the Atlantic, lends credence to this hypothesis. The prey naïveté explanation is
316 also supported by the larger prey size accessed by invasive lionfish. It is possible that, because
317 prey in the Pacific are more likely to recognize lionfish as predators, only the smallest and/or
318 least mobile species and individuals are vulnerable to predation. Still further evidence of prey
319 naïveté in the invaded range comes from differences in the use of blowing behavior by lionfish.
320 Lionfish employed blowing while stalking prey three times more often in the native Pacific range
321 compared to the invaded Atlantic range. Blowing behavior may confuse prey and facilitate head-
322 first capture as prey face upcurrent (Albins & Lyons 2012). Greater use of this hunting technique
323 may be required in the Pacific because prey recognize lionfish and are more wary. In contrast,
324 because lionfish are new to the Atlantic, they need not employ such secondary hunting methods
325 as frequently to capture naïve Atlantic prey. Given that native prey can adapt to invasive
15 326 predators by rapid evolution of behavioral responses to predator presence (Schlaepfer et al. 2005,
327 Freeman & Byers 2006), we suggest that future research focus on whether invasive lionfish and
328 native prey alter their attack and evasion behavior, respectively, through time.
329 A third explanation for increased diet breadth in invasive relative to native lionfish is the
330 competitive and/or predatory release that often accompanies invasions (Mack et al. 2000). For
331 example, the introduced grouper Cephalopholis argus fed on larger prey as a response to lower
332 competitor densities in non-native vs. native reefs (Meyer & Dierking 2011). A similar pattern
333 could affect lionfish hunting, given the larger prey sizes consumed at invaded reefs and the
334 higher diversity of ecologically similar reef fishes (i.e., potential competitors) in the native
335 Pacific relative to the invaded Atlantic (Roberts et al. 2002). Additionally, Albins (2012) has
336 demonstrated that invasive lionfish compete effectively with native grouper. Regarding release
337 from predation, although venomous spines appear to be an effective prey defense for larger
338 lionfish (Allen & Eschmeyer 1973), we hypothesize that new lionfish recruits (which have
339 flexible spines with less venom) may be the target of co-evolved, specialized, smaller predatory
340 fishes in the Pacific that do not occur in the Atlantic, thereby providing a source of biotic control
341 that is absent in the Atlantic.
342 Conclusions
343 Generally, lionfish are crepuscular predators in both their native Pacific and invaded
344 Atlantic ranges. Invasive lionfish seem to have maintained their native behaviors that generally
345 vary with environmental conditions, and therefore display no major inter-ocean differences in
346 overall activity patterns. Lionfish nonetheless exhibit substantial behavioral and ecological
347 differences between Pacific and Atlantic locations. First, invasive lionfish spend far less time
348 using blowing behavior, perhaps indicating prey naïveté in the Atlantic. Second, invasive
16 349 lionfish have far broader diets (measured by kill rates) despite the fact that (a) native lionfish
350 hunted greater variety of prey, and (b) the Pacific Ocean supports a far greater species diversity
351 of potential prey reef fishes. Importantly, only invasive lionfish were observed consuming
352 ecologically important parrotfishes. Third, Atlantic prey of lionfish are larger, even though prey
353 consumption rates are comparable to native Pacific lionfish, therefore implying that invasive
354 lionfish ingest a greater daily ration in terms of prey biomass than do native lionfish. Overall, it
355 is clear that red lionfish display a substantial capacity for behavioral adaptation to local
356 environmental conditions, likely contributing to their enormous success as an invasive species.
357 358 Acknowledgements: We are immensely grateful to Jason Miller, Dioscoro Inocencio, and Gabe
359 Scheer for help with field work, Kurt Ingeman for reviewing the manuscript, and Mark Albins
360 for general advice. Staffs of the Perry Institute for Marine Science (Bahamas) and the Central
361 Caribbean Marine Institute (Caymans) provided logistic support. Rene Abesamis and Renclar
362 Jadloc assisted with logistics in the Philippines. Statistical advice from Andrew Halford and
363 Alexander Kerr was invaluable for dealing with a complex dataset. This research was funded by
364 U.S. National Science Foundation grants 08-51162 and 12-33027 to MAH, and a UOG
365 Micronesian Area Research Center (MARC) scholarship to KC.
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21 533 534 535 536 537 538 539 540 541 542 Table 1. Results of logistic regressions of lionfish time budgets between the native Pacific
Ocean and the invaded Atlantic Ocean, using a general linear mixed-effects model (GLMM).
Shown are coefficient estimates for each explanatory variable (ß) together with standard errors
(SE), significance (p) and odd ratios (eß). Also presented are the independent effects of each
explanatory variable (%) on the dependent variable (lionfish behavior), calculated by hierarchical
partitioning. P values in bold italics are significant. Likelihood ratio and chi-square test statistics
indicate logistic regression model fit. Reference levels for this regression were set as Atlantic for
ocean, sunrise for time period, hard coral for habitat, clear for weather, and high for current.
Coefficient Intercept Ocean Pacific Time Period Morning Midday Afternoon Sunset Habitat other rock‐boulder sand‐rubble Cloud cover overcast partly cloudy Current low medium Size Depth Likelihood ratio test statistic Pearson Chi‐square 543 Estimate (ß)
‐0.003 0.438 ‐2.557 ‐2.446 ‐1.748 ‐0.719 0.434 ‐0.479 0.451 0.687 ‐0.158 1.210 1.125 ‐0.014 0.028 SE 0.773 0.891 0.244 0.279 0.216 0.271 0.259 0.239 0.271 0.227 0.184 0.326 0.346 0.013 0.024 p eß 0.997 0.623 1.549 <0.001 0.078 <0.001 0.087 <0.001 0.174 0.008 0.487 0.094 1.543 0.045 0.619 0.096 1.569 0.002 1.988 0.389 0.854 <0.001 3.355 0.001 3.079 0.102 0.258 0.499 0.241 420.736, p<0.001 1092.019, p=0.727 Independent effects (%) 3.754 35.626 13.715 7.567 9.570 10.055 19.712 22 544 545 546 547 548 549 550 Table 2. Reef-fish and crustacean prey targeted by lionfish (based on strikes, but not necessarily
kills) while hunting in their native Pacific (Philippines, Guam) and the invaded Atlantic (Cayman
Islands, Bahamas). Shown are species (or taxa when species identification was not possible)
targeted with an indication of whether each prey type was accessible to lionfish in the Atlantic,
Pacific or both, and with their respective species specific successful kill rates. The unidentified
category includes both fishes and crustaceans. PACIFIC (Pac.) ATLANTIC (Atl.) Philippines
Guam Caymans Bahamas Access In % Success % Success % Success % Success Mysidacea Both ‐ ‐ 50 ‐ Osteichthyes Acanthuridae Acanthurus nigricans Pac. ‐ 0 ‐ ‐ Apogonidae Apogon townsendi Atl. ‐ ‐ 100 ‐ Apogon sp. Pac. 0 0 ‐ ‐ Cheilodipterus sp. Pac. 0 ‐ ‐ ‐ Subphylum/ Superclass Family Species/taxa Crustacea Blenniidae Malacoctenus triangulatus Atl. ‐ ‐ 100 ‐ Pac. ‐ 0 ‐ ‐ Gobiidae Meiacanthus atrodorsalis Coryphopterus glaucofraenum ‐ ‐ 100 75 Unidentified goby Both 0 0 100 ‐ Grammatidae Gramma loreto Atl. ‐ ‐ 0 ‐ Labridae Halichoeres bivittatus Atl. ‐ ‐ ‐ 50 Halichoeres garnoti Atl. ‐ ‐ 100 0 Labroides dimidiatus Pac. 0 ‐ ‐ ‐ Thalassoma bifasciatum Atl. ‐ ‐ ‐ 33 Plotosidae Plotosus lineatus Pac. 0 ‐ ‐ ‐ Pomacentridae Chromis recruits Pac. 50 ‐ ‐ ‐ Pomacentrus coelestis Pac. ‐ 0 ‐ ‐ Stegastes partitus Atl. ‐ ‐ ‐ 100 Scaridae Scarus iserti Atl. ‐ ‐ ‐ 75 Sparisoma aurofrenatum Atl. ‐ ‐ ‐ 100 Unidentified parrotfish Atl. ‐ ‐ 0 ‐ Serranidae Serranus tigrinus Atl. ‐ ‐ 0 ‐ Tetraodontidae Canthigaster rostrata Atl. ‐ ‐ 0 0 Trichonotidae Trichonotus elegans Pac. 100 ‐ ‐ ‐ Both 36.2 29.2 20.9 22.7 Unidentified Atl. 23 551 552 553 554 Fig. 1. Regions samp
pled: the Phiilippines and
d Guam in thhe Pacific Ocean, and thhe Cayman
ntic Ocean.
Islands and Bahamass in the Atlan
24 Mean proportion of time (+SE)
1.00
Inactive
MinAct
Active
Hunting
0.90
0.80
0.70
0.60
0.50
0.40
0.30
0.20
0.10
0.00
Philippines
n=221
PACIFIC
555 556 557 558 Guam
n=167
Cayman Islands
n=439
Bahamas
n=324
ATLANTIC
Fig. 2. Time budget summaries for lionfish in each of four regions, two per ocean. Shown are
mean proportions (± SEM, n = number of 10-minute samples) of dawn-to-dusk time in each of
the four activities recorded (inactive, minimal activity [MinAct], active and hunting). 25 559 Philippines
C
Inactive
Hunting
Mean proportion of time (+SE)
1
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
1
Mean proportion of time (+SE)
A
Sunrise* Morning
n= 66
n= 26
n= 70
0.7
0.6
0.5
0.4
0.3
0.2
0.1
Sunrise* Morning
n= 94
n= 33
D
Guam
1
Mean proportion of time (+SE)
0.8
Midday Afternoon Sunset
Inactive
0.9
Hunting
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
1
Mean proportion of time (+SE)
n= 26
n= 88
Midday Afternoon
Sunset
n= 85
n= 48
n= 124
Bahamas
Inactive
Hunting
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
0
Sunrise* Morning
n= 40
560 561 562 563 564 565 566 567 568 Inactive
Hunting
0.9
0
0
B
Cayman Islands
n= 42
Midday Afternoon
n= 11
PACIFIC
n= 36
Sunset
n= 38
Sunrise* Morning
n= 72
n= 71
Midday Afternoon
n= 24
n= 137
Sunset
n= 20
ATLANTIC
Fig. 3. Time budgets of lionfish across time of day for inactivity and hunting behavior at each of
the four regions: (A) Philippines , (B) Guam, (C) Cayman Islands, and (D) Bahamas. Shown are
mean proportions (± SEM) of time spent in each behavior, standardized to regional sunrise and
sunset times: Sunrise = sunrise to 2 hr after sunrise, Morning = 2 to 5 hr after sunrise, Midday =
ca. 3-hour period midway between sunrise and sunset, Afternoon = 2 to 5 hr before sunset,
Sunset = 2 hr before sunset to sunset. n = # of 10-min samples. Asterisk (*) next to sunrise
represents significant differences in activity levels for this time period (p < 0.01; see GLMM
results Table 1).
26 569 0.50
Kills
Strikes
Mean rate (#/10 mins +SE)
0.45
A
0.40
0.35
0.30
0.25
0.20
0.15
0.10
0.05
0.00
Philippines
Guam
Cayman Islands
Little Cayman
Bahamas
0.8
Mean blow rate (#blows/10 min +SE)
0.7
a
a
0.6
B
0.5
0.4
0.3
b
0.2
b
0.1
0
Philippines
Guam
PACIFIC
570 571 572 573 574 575 Cayman Islands
Little Cayman
Bahamas
ATLANTIC
Fig. 4. Comparison of: (A) mean ( SEM) strike rates (successful and unsuccessful) and kill
rates (successful strikes, i.e. prey consumed), and (B) mean ( SEM) blow rate of lionfish in the
Pacific (left) and Atlantic (right). For (B) letters denote significant differences in blow rates
between Pacific and Atlantic Oceans (Pseudo-F = 13.234, df = 1, 1113, p = 0.001).
27 576 577 578 579 580 581 582 583 Fig 5. Mean
M
proporttion of time (± SEM) liionfish spennt inactive oor hunting inn relation too: (A)
cloud cov
ver (C = cleaar, PC = parrtly cloudy, O = overcastt), (B) waterr current leveel (L = low,, M =
medium, H = high)), and (C) habitat
h
(HC
C = hard cooral, RBC = rock-bouldder/cave, SR
RB =
sand/rubb
ble) in the native
n
Pacificc (left) and invaded
i
Atlaantic (right). Asterisks nnext to letterrs (H,
O and RBC)
R
represent significaant differencces in overaall activity levels at this level for each
environm
mental factorr (p< 0.05; seee GLMM reesults Table 1).
28 40.00
35.00
% Independent effects
30.00
25.00
20.00
15.00
10.00
5.00
0.00
584 585 586 587 588 589 590 Time*
Period
Depth
Habitat *
Size
Current*
Cloud *
cover
Ocean
Fig. 6. The percent contribution of each explanatory environmental variable to the total variation
in lionfish behavior detected by the hierarchical partitioning analyses of the logistic regression
model (see Table S1 in the Supplement). Asterisks next to variables indicate which variables
were significant in the logistic model.